Stress-activated MAPK signalling controls fission yeast actomyosin ring integrity by modulating formin For3 levels

  1. Elisa Gómez-Gil
  2. Rebeca Martín-García
  3. Jero Vicente-Soler
  4. Alejandro Franco
  5. Beatriz Vázquez-Marín
  6. Francisco Prieto-Ruiz
  7. Teresa Soto
  8. Pilar Pérez
  9. Marisa Madrid  Is a corresponding author
  10. Jose Cansado  Is a corresponding author
  1. Universidad de Murcia, Spain
  2. Instituto de Biología Funcional y Genómica/Universidad de Salamanca, Spain

Abstract

Cytokinesis, which enables the physical separation of daughter cells once mitosis has been completed, is executed in fungal and animal cells by a contractile actin- and myosin-based ring (CAR). In the fission yeast Schizosaccharomyces pombe the formin For3 nucleates actin cables and also co-operates for CAR assembly during cytokinesis. Mitogen-Activated Protein Kinases (MAPKs) regulate essential adaptive responses in eukaryotic organisms to environmental changes. We show that the Stress Activated Protein Kinase pathway (SAPK) and its effector, MAPK Sty1, downregulates CAR assembly in S. pombe when its integrity becomes compromised during cytoskeletal damage and stress by reducing For3 levels. Accurate control of For3 levels by the SAPK pathway may thus represent a novel regulatory mechanism of cytokinesis outcome in response to environmental cues. Conversely, SAPK signalling favours CAR assembly and integrity in its close relative S. japonicus, revealing a remarkable evolutionary divergence of this response within the fission yeast clade.

Data availability

All data generated or analysed during this study are included within the manuscript and supporting files.

Article and author information

Author details

  1. Elisa Gómez-Gil

    Genetics and Microbiology, Universidad de Murcia, Murcia, Spain
    Competing interests
    The authors declare that no competing interests exist.
  2. Rebeca Martín-García

    Morfogénesis y Polaridad Celular, Instituto de Biología Funcional y Genómica/Universidad de Salamanca, Salamanca, Spain
    Competing interests
    The authors declare that no competing interests exist.
  3. Jero Vicente-Soler

    Genetics and Microbiology, Universidad de Murcia, Murcia, Spain
    Competing interests
    The authors declare that no competing interests exist.
  4. Alejandro Franco

    Genetics and Microbiology, Universidad de Murcia, Murcia, Spain
    Competing interests
    The authors declare that no competing interests exist.
  5. Beatriz Vázquez-Marín

    Genetics and Microbiology, Universidad de Murcia, Murcia, Spain
    Competing interests
    The authors declare that no competing interests exist.
  6. Francisco Prieto-Ruiz

    Genetics and Microbiology, Universidad de Murcia, Murcia, Spain
    Competing interests
    The authors declare that no competing interests exist.
  7. Teresa Soto

    Genetics and Microbiology, Universidad de Murcia, Murcia, Spain
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2965-318X
  8. Pilar Pérez

    Morfogénesis y Polaridad Celular, Instituto de Biología Funcional y Genómica/Universidad de Salamanca, Salamanca, Spain
    Competing interests
    The authors declare that no competing interests exist.
  9. Marisa Madrid

    Genetics and Microbiology, Universidad de Murcia, Murcia, Spain
    For correspondence
    marisa@um.es
    Competing interests
    The authors declare that no competing interests exist.
  10. Jose Cansado

    Genetics and Microbiology, Universidad de Murcia, Murcia, Spain
    For correspondence
    jcansado@um.es
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2342-8152

Funding

Ministerio de Economía y Competitividad (BFU2017-82423-P)

  • Jose Cansado

Ministerio de Economía y Competitividad (PGC2018-098924-B-100)

  • Pilar Pérez

Junta de Castilla y Leon (CLU-2017-03)

  • Pilar Pérez

Fundacion Seneca (20856/PI/18)

  • Jose Cansado

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

© 2020, Gómez-Gil et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 1,818
    views
  • 277
    downloads
  • 17
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Elisa Gómez-Gil
  2. Rebeca Martín-García
  3. Jero Vicente-Soler
  4. Alejandro Franco
  5. Beatriz Vázquez-Marín
  6. Francisco Prieto-Ruiz
  7. Teresa Soto
  8. Pilar Pérez
  9. Marisa Madrid
  10. Jose Cansado
(2020)
Stress-activated MAPK signalling controls fission yeast actomyosin ring integrity by modulating formin For3 levels
eLife 9:e57951.
https://doi.org/10.7554/eLife.57951

Share this article

https://doi.org/10.7554/eLife.57951

Further reading

    1. Cell Biology
    2. Developmental Biology
    Sofía Suárez Freire, Sebastián Perez-Pandolfo ... Mariana Melani
    Research Article

    Eukaryotic cells depend on exocytosis to direct intracellularly synthesized material toward the extracellular space or the plasma membrane, so exocytosis constitutes a basic function for cellular homeostasis and communication between cells. The secretory pathway includes biogenesis of secretory granules (SGs), their maturation and fusion with the plasma membrane (exocytosis), resulting in release of SG content to the extracellular space. The larval salivary gland of Drosophila melanogaster is an excellent model for studying exocytosis. This gland synthesizes mucins that are packaged in SGs that sprout from the trans-Golgi network and then undergo a maturation process that involves homotypic fusion, condensation, and acidification. Finally, mature SGs are directed to the apical domain of the plasma membrane with which they fuse, releasing their content into the gland lumen. The exocyst is a hetero-octameric complex that participates in tethering of vesicles to the plasma membrane during constitutive exocytosis. By precise temperature-dependent gradual activation of the Gal4-UAS expression system, we have induced different levels of silencing of exocyst complex subunits, and identified three temporarily distinctive steps of the regulated exocytic pathway where the exocyst is critically required: SG biogenesis, SG maturation, and SG exocytosis. Our results shed light on previously unidentified functions of the exocyst along the exocytic pathway. We propose that the exocyst acts as a general tethering factor in various steps of this cellular process.

    1. Cell Biology
    2. Developmental Biology
    Heungjin Ryu, Kibum Nam ... Jung-Hoon Park
    Research Article

    In most murine species, spermatozoa exhibit a falciform apical hook at the head end. The function of the sperm hook is not yet clearly understood. In this study, we investigate the role of the sperm hook in the migration of spermatozoa through the female reproductive tract in Mus musculus (C57BL/6), using a deep tissue imaging custom-built two-photon microscope. Through live reproductive tract imaging, we found evidence indicating that the sperm hook aids in the attachment of spermatozoa to the epithelium and facilitates interactions between spermatozoa and the epithelium during migration in the uterus and oviduct. We also observed synchronized sperm beating, which resulted from the spontaneous unidirectional rearrangement of spermatozoa in the uterus. Based on live imaging of spermatozoa-epithelium interaction dynamics, we propose that the sperm hook plays a crucial role in successful migration through the female reproductive tract by providing anchor-like mechanical support and facilitating interactions between spermatozoa and the female reproductive tract in the house mouse.